Dataset Information

Deeply-sourced formate fuels sulfate reducers but not methanogens at Lost City hydrothermal field.

ABSTRACT: Hydrogen produced during water-rock serpentinization reactions can drive the synthesis of organic compounds both biotically and abiotically. We investigated abiotic carbon production and microbial metabolic pathways at the high energy but low diversity serpentinite-hosted Lost City hydrothermal field. Compound-specific 14C data demonstrates that formate is mantle-derived and abiotic in some locations and has an additional, seawater-derived component in others. Lipids produced by the dominant member of the archaeal community, the Lost City Methanosarcinales, largely lack 14C, but metagenomic evidence suggests they cannot use formate for methanogenesis. Instead, sulfate-reducing bacteria may be the primary consumers of formate in Lost City chimneys. Paradoxically, the archaeal phylotype that numerically dominates the chimney microbial communities appears ill suited to live in pure hydrothermal fluids without the co-occurrence of organisms that can liberate CO2. Considering the lack of dissolved inorganic carbon in such systems, the ability to utilize formate may be a key trait for survival in pristine serpentinite-hosted environments.

SUBMITTER: Lang SQ

PROVIDER: S-EPMC5768773 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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Deeply-sourced formate fuels sulfate reducers but not methanogens at Lost City hydrothermal field.

Lang Susan Q SQ Früh-Green Gretchen L GL Bernasconi Stefano M SM Brazelton William J WJ Schrenk Matthew O MO McGonigle Julia M JM

Scientific reports 20180115 1

Hydrogen produced during water-rock serpentinization reactions can drive the synthesis of organic compounds both biotically and abiotically. We investigated abiotic carbon production and microbial metabolic pathways at the high energy but low diversity serpentinite-hosted Lost City hydrothermal field. Compound-specific <sup>14</sup>C data demonstrates that formate is mantle-derived and abiotic in some locations and has an additional, seawater-derived component in others. Lipids produced by the d ...[more]

PMID: 29335466

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Project description:Extremely thermophilic methanogens in the Methanococci and heterotrophs in the Thermococci are common in deep-sea hydrothermal vents. All Methanococci use H2 as an electron donor, and a few species can also use formate. Most Methanococci have a coenzyme F420-reducing formate dehydrogenase. All Thermococci reduce S0 but have hydrogenases and produce H2 in the absence of S0. Some Thermococci have formate hydrogenlyase (Fhl) that reversibly converts H2 and CO2 to formate or an NAD(P)+-reducing formate dehydrogenase (Nfd). Questions remain if Methanococci or Thermococci use or produce formate in nature, why only certain species can grow on or produce formate, and what the physiological role of formate is? Formate forms abiotically in hydrothermal fluids through chemical equilibrium with primarily H2, CO2, and CO and is strongly dependent upon H2 concentration, pH, and temperature. Formate concentrations are highest in hydrothermal fluids where H2 concentrations are also high, such as in ultramafic systems where serpentinization reactions occur. In nature, Methanococci are likely to use formate as an electron donor when H2 is limiting. Thermococci with Fhl likely convert H2 and CO2 to formate when H2 concentrations become inhibitory for growth. They are unlikely to grow on formate in nature unless formate is more abundant than H2 in the environment. Nearly all Methanococci and Thermococci have a gene for at least one formate dehydrogenase catalytic subunit, which may be used to provide free formate for de novo purine biosynthesis. However, only species with a membrane-bound formate transporter can grow on or secrete formate. Interspecies H2 transfer occurs between Thermococci and Methanococci. This and putative interspecies formate transfer may support Methanococci in low H2 environments, which in turn may prevent growth inhibition of Thermococci by its own H2. Future research directions include understanding when, where, and how formate is used and produced by these organisms in nature, and how transcription of Thermococci genes encoding formate-related enzymes are regulated.

Project description:Elucidating the in situ metabolic activity of phylogenetically diverse populations of sulfate-reducing microorganisms that populate anoxic sedimentary environments is key to understanding subsurface ecology. Previous pure culture studies have demonstrated that the transcript abundance of dissimilatory (bi)sulfite reductase genes is correlated with the sulfate-reducing activity of individual cells. To evaluate whether expression of these genes was diagnostic for subsurface communities, dissimilatory (bi)sulfite reductase gene transcript abundance in phylogenetically distinct sulfate-reducing populations was quantified during a field experiment in which acetate was added to uranium-contaminated groundwater. Analysis of dsrAB sequences prior to the addition of acetate indicated that Desulfobacteraceae, Desulfobulbaceae, and Syntrophaceae-related sulfate reducers were the most abundant. Quantifying dsrB transcripts of the individual populations suggested that Desulfobacteraceae initially had higher dsrB transcripts per cell than Desulfobulbaceae or Syntrophaceae populations and that the activity of Desulfobacteraceae increased further when the metabolism of dissimilatory metal reducers competing for the added acetate declined. In contrast, dsrB transcript abundance in Desulfobulbaceae and Syntrophaceae remained relatively constant, suggesting a lack of stimulation by added acetate. The indication of higher sulfate-reducing activity in the Desulfobacteraceae was consistent with the finding that Desulfobacteraceae became the predominant component of the sulfate-reducing community. Discontinuing acetate additions resulted in a decline in dsrB transcript abundance in the Desulfobacteraceae. These results suggest that monitoring transcripts of dissimilatory (bi)sulfite reductase genes in distinct populations of sulfate reducers can provide insight into the relative rates of metabolism of different components of the sulfate-reducing community and their ability to respond to environmental perturbations.

Dataset Information

Deeply-sourced formate fuels sulfate reducers but not methanogens at Lost City hydrothermal field.

Publications

Deeply-sourced formate fuels sulfate reducers but not methanogens at Lost City hydrothermal field.

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